Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA 71:209–249. https://doi.org/10.3322/caac.21660

Article  CAS  PubMed  Google Scholar 

Redig AJ, McAllister SS (2013) Breast cancer as a systemic disease: a view of metastasis. J Intern Med 274:113–126. https://doi.org/10.1111/joim.12084

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pantel K, Brakenhoff RH (2004) Dissecting the metastatic cascade. Nat Rev Cancer 4:448–456. https://doi.org/10.1038/nrc1370

Article  CAS  PubMed  Google Scholar 

Wu Y, Sarkissyan M, Vadgama JV (2016) Epithelial-mesenchymal transition and breast cancer. J Clin Med 5:13. https://doi.org/10.3390/jcm5020013

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ye X, Brabletz T, Kang Y, Longmore GD, Nieto MA, Stanger BZ, Yang J, Weinberg RA (2017) Upholding a role for EMT in breast cancer metastasis. Nature 547:E1–E3. https://doi.org/10.1038/nature22816

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hunter KW, Crawford NPS, Alsarraj J (2008) Mechanisms of metastasis. Breast Cancer Res 10:S2. https://doi.org/10.1186/bcr1988

Article  PubMed  PubMed Central  Google Scholar 

Mina LA, Sledge GW (2011) Rethinking the metastatic cascade as a therapeutic target. Nat Rev Clin Oncol 8:325–332. https://doi.org/10.1038/nrclinonc.2011.59

Article  CAS  PubMed  Google Scholar 

Lu X, Kang Y (2007) Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 12:153–162. https://doi.org/10.1007/s10911-007-9047-3

Article  PubMed  Google Scholar 

Chen W, Hoffmann AD, Liu H, Liu X (2018) Organotropism: new insights into molecular mechanisms of breast cancer metastasis. NPJ Precis Oncol 2: 4. https://doi.org/10.1038/s41698-018-0047-0

Wei S, Siegal GP (2017) Metastatic organotropism: an intrinsic property of breast cancer molecular subtypes. Adv Anat Pathol 24:78–81

Article  CAS  PubMed  Google Scholar 

Wong GL, Abu Jalboush S, Lo H-W (2020) Exosomal microRNAs and organotropism in breast cancer metastasis. Cancers 12:1827

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mo Z, Cheong JYA, Xiang L, Le MTN, Grimson A, Zhang DX (2021) Extracellular vesicle-associated organotropic metastasis. Cell Prolif 54:e12948. https://doi.org/10.1111/cpr.12948

Article  PubMed  Google Scholar 

Yu T, Wang C, Xie M, Zhu C, Shu Y, Tang J, Guan X (2021) Heterogeneity of CTC contributes to the organotropism of breast cancer. Biomed Pharmacother 137:111314. https://doi.org/10.1016/j.biopha.2021.111314

Article  CAS  PubMed  Google Scholar 

Wang C, Xu K, Wang R, Han X, Tang J, Guan X (2021) Heterogeneity of BCSCs contributes to the metastatic organotropism of breast cancer. J Exp Clin Cancer Res 40:370. https://doi.org/10.1186/s13046-021-02164-6

Article  CAS  PubMed  PubMed Central  Google Scholar 

Smith HA, Kang Y (2017) Determinants of organotropic metastasis. Annu Rev Cancer Biol 1:403–423. https://doi.org/10.1146/annurev-cancerbio-041916-064715

Article  Google Scholar 

Waza AA, Tarfeen N, Majid S, Hassan Y, Mir R, Rather MY, Shah NUD (2021) Metastatic breast cancer, organotropism and therapeutics: a review. Curr Cancer Drug Targets 21:813–828. https://doi.org/10.2174/1568009621666210806094410

Article  CAS  PubMed  Google Scholar 

Blows FM, Driver KE, Schmidt MK, Broeks A, van Leeuwen FE, Wesseling J, Cheang MC, Gelmon K, Nielsen TO, Blomqvist C, Heikkila P, Heikkinen T, Nevanlinna H, Akslen LA, Begin LR, Foulkes WD, Couch FJ, Wang X, Cafourek V, Olson JE, Baglietto L, Giles GG, Severi G, McLean CA, Southey MC, Rakha E, Green AR, Ellis IO, Sherman ME, Lissowska J, Anderson WF, Cox A, Cross SS, Reed MW, Provenzano E, Dawson SJ, Dunning AM, Humphreys M, Easton DF, Garcia-Closas M, Caldas C, Pharoah PD, Huntsman D (2010) Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies. PLoS Med 7:e1000279. https://doi.org/10.1371/journal.pmed.1000279

Article  PubMed  PubMed Central  Google Scholar 

DeSantis CE, Ma J, Goding Sauer A, Newman LA, Jemal A (2017) Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin 67:439–448. https://doi.org/10.3322/caac.21412

Article  PubMed  Google Scholar 

Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38:1289–1297. https://doi.org/10.1038/ng1901

Article  CAS  PubMed  Google Scholar 

Chu D, Paoletti C, Gersch C, VanDenBerg DA, Zabransky DJ, Cochran RL, Wong HY, Toro PV, Cidado J, Croessmann S, Erlanger B, Cravero K, Kyker-Snowman K, Button B, Parsons HA, Dalton WB, Gillani R, Medford A, Aung K, Tokudome N, Chinnaiyan AM, Schott A, Robinson D, Jacks KS, Lauring J, Hurley PJ, Hayes DF, Rae JM, Park BH (2016) ESR1 mutations in circulating plasma tumor DNA from metastatic breast cancer patients. Clin Cancer Res 22:993–999. https://doi.org/10.1158/1078-0432.CCR-15-0943

Article  CAS  PubMed  Google Scholar 

Spoerke JM, Gendreau S, Walter K, Qiu J, Wilson TR, Savage H, Aimi J, Derynck MK, Chen M, Chan IT, Amler LC, Hampton GM, Johnston S, Krop I, Schmid P, Lackner MR (2016) Heterogeneity and clinical significance of ESR1 mutations in ER-positive metastatic breast cancer patients receiving fulvestrant. Nat Commun 7:11579. https://doi.org/10.1038/ncomms11579

Article  PubMed  PubMed Central  Google Scholar 

Guttery DS, Page K, Hills A, Woodley L, Marchese SD, Rghebi B, Hastings RK, Luo J, Pringle JH, Stebbing J, Coombes RC, Ali S, Shaw JA (2015) Noninvasive detection of activating estrogen receptor 1 (ESR1) mutations in estrogen receptor-positive metastatic breast cancer. Clin Chem 61:974–982. https://doi.org/10.1373/clinchem.2015.238717

Article  CAS  PubMed  Google Scholar 

Razavi P, Chang MT, Xu G, Bandlamudi C, Ross DS, Vasan N, Cai Y, Bielski CM, Donoghue MTA, Jonsson P, Penson A, Shen R, Pareja F, Kundra R, Middha S, Cheng ML, Zehir A, Kandoth C, Patel R, Huberman K, Smyth LM, Jhaveri K, Modi S, Traina TA, Dang C, Zhang W, Weigelt B, Li BT, Ladanyi M, Hyman DM, Schultz N, Robson ME, Hudis C, Brogi E, Viale A, Norton L, Dickler MN, Berger MF, Iacobuzio-Donahue CA, Chandarlapaty S, Scaltriti M, Reis-Filho JS, Solit DB, Taylor BS, Baselga J (2018) The genomic landscape of endocrine-resistant advanced breast cancers. Cancer Cell 34:427-438.e426. https://doi.org/10.1016/j.ccell.2018.08.008

Article  CAS  PubMed  PubMed Central  Google Scholar 

Arnesen S, Blanchard Z, Williams MM, Berrett KC, Li Z, Oesterreich S, Richer JK, Gertz J (2021) Estrogen receptor alpha mutations in breast cancer cells cause gene expression changes through constant activity and secondary effects. Cancer Res 81:539. https://doi.org/10.1158/0008-5472.CAN-20-1171

Article  CAS  PubMed  Google Scholar 

Toy W, Shen Y, Won H, Green B, Sakr RA, Will M, Li Z, Gala K, Fanning S, King TA, Hudis C, Chen D, Taran T, Hortobagyi G, Greene G, Berger M, Baselga J, Chandarlapaty S (2013) ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet 45:1439–1445. https://doi.org/10.1038/ng.2822

Article  CAS  PubMed  PubMed Central  Google Scholar 

Harrod A, Fulton J, Nguyen VT, Periyasamy M, Ramos-Garcia L, Lai C-F, Metodieva G, de Giorgio A, Williams RL, Santos DB (2017) Genomic modelling of the ESR1 Y537S mutation for evaluating function and new therapeutic approaches for metastatic breast cancer. Oncogene 36:2286

Article  CAS  PubMed  Google Scholar 

Bahreini A, Li Z, Wang P, Levine KM, Tasdemir N, Cao L, Weir HM, Puhalla SL, Davidson NE, Stern AM (2017) Mutation site and context dependent effects of ESR1 mutation in genome-edited breast cancer cell models. Breast Cancer Res 19:60

Article  PubMed  PubMed Central  Google Scholar 

Merenbakh-Lamin K, Ben-Baruch N, Yeheskel A, Dvir A, Soussan-Gutman L, Jeselsohn R, Yelensky R, Brown M, Miller VA, Sarid D (2013) D538G mutation in estrogen receptor-α: a novel mechanism for acquired endocrine resistance in breast cancer. Cancer Res 73:6856–6864

Article  CAS  PubMed  Google Scholar 

Weis KE, Ekena K, Thomas JA, Lazennec G, Katzenellenbogen BS (1996) Constitutively active human estrogen receptors containing amino acid substitutions for tyrosine 537 in the receptor protein. Mol Endocrinol 10:1388–1398. https://doi.org/10.1210/mend.10.11.8923465

Article  CAS  PubMed  Google Scholar 

Li Z, Wu Y, Yates ME, Tasdemir N, Bahreini A, Chen J, Levine KM, Priedigkeit NM, Nasrazadani A, Ali S, Buluwela L, Arnesen S, Gertz J, Richer JK, Troness B, El-Ashry D, Zhang Q, Gerratana L, Zhang Y, Cristofanilli M, Montanez MA, Sundd P, Wallace CT, Watkins SC, Fumagalli C, Guerini-Rocco E, Zhu L, Tseng GC, Wagle N, Carroll JS, Jank P, Denkert C, Karsten MM, Blohmer JU, Park BH, Lucas PC, Atkinson JM, Lee AV, Oesterreich S (2022) Hotspot ESR1 mutations are multimodal and contextual modulators of breast cancer metastasis. Cancer Res. https://doi.org/10.1158/0008-5472.Can-21-2576

Article  PubMed  PubMed Central  Google Scholar 

Jeselsohn R, Bergholz JS, Pun M, Cornwell M, Liu W, Nardone A, Xiao T, Li W, Qiu X, Buchwalter G (2018) Allele-specific chromatin recruitment and therapeutic vulnerabilities of ESR1 activating mutations. Cancer Cell 33(173–186):e175

Google Scholar 

Zinger L, Merenbakh-Lamin K, Klein A, Elazar A, Journo S, Boldes T, Pasmanik-Chor M, Spitzer A, Rubinek T, Wolf I (2019) Ligand-binding domain-activating mutations of ESR1 rewire cellular metabolism of breast cancer cells. Clin Cancer Res 25:2900–2914.